Radiographic assessment of osteoarthritis in population studies: whither kellgren and lawrence?

Osteoarthritis and Cartilage (1993) 1, 203-206 © 1993 Osteoarthritis Research Society

1063-4584/93/040203 + 04 $08.00/0

OSTEOARTHRITIS and CARTILAGE EDITORIAL

R a d i o g r a p h i c a s s e s s m e n t of o s t e o a r t h r i t i s in p o p u l a t i o n s t u d i e s : w h i t h e r K e l l g r e n and L a w r e n c e ? BY TIM D. SPECTOR* AND CYRUS COOPER t

*The Department of Rheumatology, St Thomas" Hospital, Lambeth Palace Road, London SE1 7EH, U.K. t M R C Environmental Epidemiology Unit, Southampton General Hospital, Southampton S 0 9 4XY, U.K. Key words: Epidemiology, Definition, Osteoarthritis, Knee, Hip.

OSTEOARTHRITIS (OA) is the most frequent joint disorder in the world today, yet it remains an enigma to the clinician, the epidemiologist, the radiologist and the cell biologist. The term describes a complex disease process in which a combination of systemic and local mechanisms result in c h a r a c t e r i s t i c pathological and radiological changes. These abnormalities are often, but not always, associated with symptoms and disability. Definitions of o s t e o a r t h r i t i s may therefore be based upon any combination of clinical features, r a d i o g r a p h i c changes and pathological findings, be they in joint tissue, synovial fluid or blood. These definitions can be put to a myriad of different uses. Among the most important, is classification of individuals as being with, or without, the condition for the purposes of etiologic or t h e r a p e u t i c research. While the requirements of any definition in each of these two areas of inquiry are not identical, they share certain common objectives. The method should ideally be accurate, reproducible, n o n i n v a s i v e , c o n v e n i e n t and relatively inexpensive. A r a d i o g r a p h i c system for assessing o s t e o a r t h r i t i s would, if appropriately validated, meet these c r i t e r i a [1]. While the features of a radiographic scale may not completely m a t c h those used to define the osteoarthritis process at a pathological and cellular level (leading to inevitable discordance between these two types of measurement), the radiographic features which are c u r r e n t l y used to assess osteoarthritis were originally selected to measure various aspects of cartilage loss and subchondral bone reaction. These remain the pathological hallmarks of the disorder [2].

Although several r a d i o g r a p h i c grading systems have been proposed in the last 15 years [3-5], most epidemiologic studies h a v e utilized the Empire Rheumatism Council system [6] first described over three decades ago. This system, developed by Kellgren and L a w r e n c e [7], assigns one of five grades (0-4) to o s t e o a r t h r i t i s at various joint sites: knee, hip, hand and spine. Grading is performed by comparing the index r a d i o g r a p h with reproductions in a r a d i o g r a p h i c atlas [6]. The c r i t e r i a for increasing severity of o s t e o a r t h r i t i s are given in Table I, and relate to the assumed sequential Table I

The KeUgren/Lawrence grading system of osteoarthritis [6, 7] (a)

Radiologic features on which grades were based

(1) Formation of osteophytes on the joint margins or, in the case of the knee joint, on the tibial spines (2) Periarticular ossicles; these are found chiefly in relation to the distal and proximal interphalangeal joints (3) Narrowing of joint cartilage associated with sclerosis of subchondral bone (4) Small pseudocystic areas with sclerotic walls situated usually in the subchondral bone (5) Altered shape of the bone ends, particular in .... the head of the femur Co) R a d i o g r a p h i c c r i t e r i a f o r a s s e s s m e n t o f OA Grade 0 None No features of OA Grade 1 Doubtful Minute osteophyte, doubtful significance Grade 2 Minimal Definite osteophyte, unimpaired joint space Grade 3 Moderate Moderate diminution of joint space Grade 4 Severe Joint space greatly impaired with sclerosis of subchondral bone

Address correspondence to: Dr C. Cooper, MRC Environmental Epidemiology U n i t , Southampton General Hospital, Southampton SO9 4XY, U.K. 203

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S p e c t o r and Cooper: R a d i o g r a p h i c a s s e s s m e n t o f o s t e o a r t h r i t i s

appearance of osteophytes, joint space loss, subchondral sclerosis and cyst formation. Epidemiologic studies support the notion t h a t any radiographic grading system for osteoarthritis should be joint specific [8]. The age and sexspecific prevalence of osteoarthritis, the individual risk factors for the condition, and the relationship between radiographic change and symptoms are all known to differ according to joint site [9-12]. There are, however, several reasons why the Kellgren/Lawrence scales may require a re-appraisal. Most notable among these are (1) inconsistencies in the descriptions of radiographic features of osteoarthritis by Kellgren and Lawrence themselves and (2) the prominence awarded to the osteophyte at all joint sites. We discuss these deficiencies with specific reference to the knee and hip, before highlighting alternative approaches to radiographic definition of osteoarthritis. Although the original intention of the system was t h a t grades be defined by standard radiographs, the films finally chosen for the system did not easily conform to the written descriptions and the descriptions provided by the authors also varied [7,8]. Initially no specific clarification was given for the interpretation of the grades. Two years later, grade 2 for the knee was defined as ~the presence of definite osteophytes with minimal joint space narrowing' [6] and even later was interpreted as 'definite osteophytes but the joint space is unimpaired' [8]. Likewise at the hip, there are differences between the original atlas legend definition for grade 2, which reads 'definite joint space narrowing, definite osteophytes, slight sclerosis' [6] and the later version which states ~definite osteophyte, joint space unimpaired' [8]. These differences have permitted research workers to assign osteoarthritis at the hip and knee in quite different ways while still maintaining t h a t they had used standard criteria. Inconsistencies in definition must also contribute significantly to the poor between-observer and between-center reproducibility which has been reported [13-15] for the Kellgren/Lawrence system at some sites. The second potential problem with the system lies in its emphasis on the osteophyte. The precise chronological sequence of events in osteoarthritis remains uncertain, and it is not clear whether the primary event occurs in subchondral bone or articular cartilage [16]. Two of the four grades in the revised Kellgren/Lawrence scheme refer only to osteophytes. An individual with joint space narrowing but no visible osteophytes cannot, according to our interpretation, be classified as having OA of the hip or knee using the

Kellgren/Lawrence system. The system therefore assumes t h a t joint space loss occurs after osteophytosis, and has equal importance in the hip and knee. The widespread realization of these deficiencies in the current procedure for the radiographic assessment of osteoarthritis leads us to the conclusion t h a t a reappraisal is now required. This is made all the more timely with the emergence of a number of alternative approaches to the problem [1,13,14,17]. An initial step has been to break up the radiographic definition system into its component features, quantify each featdre more precisely, and assess the reproducibility and clinical correlates of each [12,17]. Studies have attempted this task at the knee [17,18], hip [14,19] and hand [20,21], respectively. For the knee, one of the studies [12] categorized each of joint space narrowing, osteophytosis and sclerosis on a 4-point scale from 0 (normal) to 3 (severe). The between- and within:observer reproducibility for the grading of each feature was assessed in a large sample of weight~bearing knee radiographs chosen to represent the full spectrum of disease. This was compared w i t h the reproducibility of the Kellgren/Lawrence scale using the Atlas of Standard Radiographs [6]. T.he ascert a i n m e n t of individual features, both betWeen and within observers, was as reproducible as t h a t of the composite Kellgren/Lawrence scale. In a preliminary analysis of 1954 knee radiographs obtained from a population sample, the discriminatory ability of various joint space measures, osteophyte, and the Kellgren/Lawrence system were compared further [18]. All measures showed good within-observer reproducibility but those scoring for the presence of definite osteophytes (including Kellgren/Lawrence grade 2 +) best predicted knee pain. These preliminary results suggest t h a t for the knee joint, osteophytes are the best predictor of clinically manifest disease, with measures of narrowing only useful for severity or progression. In a population-based study of the hip [14], six features of osteoarthritis were measured (joint space width at four points on the arc of the joint, size of the largest osteophyte, and thickness of subchondral sclerosis). A precisely delineated composite score was also evaluated. In this instance, the measures of joint space were more reproducible t h a n those of osteophyte, sclerosis or the composite score. However, the reproducibility of all the features improved when more severe cutoff levels for osteoarthritis were adopted. Minimal joint space measurement and the composite score showed similar associations with pain. These associations were stronger t h a n that between pain

Osteoarthritis and Cartilage Vol. 1 No. 4 and osteophyte, suggesting t h a t joint space appears to be of greater importance t h a n osteophyte in the definition of hip OA. The recent findings of a large epidemiological study in women confirm these observations, but suggest t h a t the addition of osteophyte to joint space narrowing significantly improves the predictive capacity of the latter measure for hip pain [22]. For the h a n d [20, 21], there are often no symptoms with which to compare radiographic features. However, K a l l m a n e t a l . [20] have devised an atlas whereby each joint can be classifled by individual features (narrowing, osteophyte, sclerosis). The reproducibility of this system was found to be similar to t h a t of the original Kellgren/Lawrence grading. An alternative approach to radiographic definition of osteoarthritis at these three joint sites has been adopted by the Subcommittee on Classification Criteria of the American College of Rheumatology [4, 17, 19, 21]. Here, the different radiographic features (joint space narrowing, osteophyte, sclerosis) are compared at different joint sites for reproducibility and ability to discriminate osteoarthritis from other joint disorders. In their studies of criteria for both knee [17] and hip [19] osteoarthritis, the Subcommittee reported t h a t osteophyte performed better t h a n joint space narrowing in distinguishing patients with painful osteoarthritis from those with knee or hip pain of other cause. In both studies the most frequent disorder in the comparison group was rheumatoid arthritis, a feature of which i s joint space narrowing on X-ray. The discriminant capacities of different radiographic features may thus depend on the population being studied. Criteria developed in symptomatic patients attending physicians will likely differ from those developed in the community. These studies suggest t h a t no single grading system (say measurement of joint space alone) is suitable for the assessment of osteoarthritis at all sites. Rather, they imply t h a t different measures might be appropriate in different circumstances. At the hip, therefore, measurement of minimal joint space is simple, reproducible and might suffice for the assignment of osteoarthritis in epidemiological studies. The same might not be true of the knee, where the precise location for any joint space measurement and the tricompartmental structure of the joint [15], make assessment of this feature more difficult and assessment of osteophyte potentially more useful. Where does this leave us with the Kellgren/Lawrence scale? It does not appear appropriate to abandon it before consensus is

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reached on a n improved method. Equally, methodologic rigour forces us to accept some of its deficiencies w i t h o u t necessarily sacrificing the principle of a composite radiographic measure of osteoarthritis. One way forward would be to publish an agreed standardized i n t e r p r e t a t i o n of the Kellgren/Lawrence grades to accompany the original radiographs. This would make it more likely t h a t centers would u s e the system in the same way. Thus, for example, grade 2 might be defined as ~presence of definite osteophytes' and grade 3 ~joint space narrowing in addition to definite osteophytes'. Whilst advocating the continued use of standardized Kellgren/Lawrence scales in epidemiologic research, we also favour the measurement of individual joint features (such as joint space), which may be more useful in certain joints, and are likely to provide more information when used prospectively. F a r from denigrating a generation of research into osteoarthritis, such a scale would vindicate the observations of our forebears in osteoarthritis epidemiology and provide a firm stage to explore further hypotheses on the etiology and prevention of this condition.

Acknowledgments This work was supported by the Arthritis and Rheumatism Council of Great Britain. We are grateful to Mrs Gill Strange for assistance in preparing the original manuscript.

References 1. Menkes CJ. Radiographic criteria for classification of osteoarthritis. J Rheumatol 1991;18(Suppl 27):13-5. 2. McAlindon TE, Dieppe P. Osteoarthritis: definitions and criteria. A n n R h e u m Dis 1989;48:531-2. 3. Lequesne M. Clinical features, diagnostic criteri a, functional assessments and radiological classifications of osteoarthritis (excluding the spine). Bailliere's Clin R h e u m a t o l 1982;7:1-10. 4. Altman RD, Fries JF, Bloch DA et al. Radiographic assessment of progression in osteoarthritis. .... A r t h r i t i s R h e u m 1987;30:1214-25. 5. Buckland-Wright C, Macfarlane D, Lynch J. Quantitative microfocal radiographic assessment of disease and progression in osteoarthritis of the hand. J R h e u m a t o l 1991;18(Suppl 27):40-1. 6. The epidemiology of chronic rheumatism. A t l a s of standard radiographs, Vol 2. Oxford: Blackwell

Scientific, 1963. 7. Kellgren JK, Lawrence JS. Radiological assessment of osteoarthritis. A n n R h e u m Dis 1957;16:494-501. 8. Lawrence JS. R h e u m a t i s m in populations. London: Heinemann 1977:99-100. 9. Felson DT, Naimark A, Anderson J, Kazis L, Castelli W, Meenan RF. The prevalence of knee

206

10.

11.

12.

13. 14. 15.

Spector and Cooper: Radiographic a s s e s s m e n t of osteoarthritis osteoarthritis in the elderly. The Framingham osteoarthritis study. A r t h r i t i s R h e u m 1987;30:9148. Van Saase JLCM, Van Romunde LKS, Cats A, Vandenbroucke JP, Valkenburg HA. Epidemiology of osteoarthritist: Zoetermeer survey. Comparison of radiological osteoarthritis in a Dutch population with that in 10 other populations. A n n R h e u m Dis 1989;48:271-80. Hochberg MC. Epidemiologic association of pain in osteoarthritis of the knee: data from the National Health and Nutrition Examination Survey and the National Health and Nutrition Examination. Vol. 1, Epidemiologic follow-up survey. S e m i n Arthritis R h e u m 1989;18(Suppl 2):4-9). Hart DJ, Spector TD, Brown P, Wilson P, Doyle DV, Silman AJ. Clinical signs of early osteoarthritis: reproducibility and relation to X-ray changes in 541 women in the general population. A n n R h e u m Dis 1991;50:467-70. Spector T, Cooper C, Cushnaghan J, H a r t DJ, Dieppe PA. A radiographic atlas of knee osteoarthritis. London: Springer Verlag 1992:1-15. Croft P, Cooper C, Wickham C, Coggon D. Defining osteoarthritis of the hip for epidemiologic studies. A m J Epidemiol 1990;132:514-22. Cooper C, Cushnagham J, Kirwan JR et al. Radiographic assessment of the knee joint in osteoarthritis. A n n R h e u m Dis 1992;51:80-2.

16. Radin EL, Burr DB, Caterson B, Fyhrie D, Brown TD, Boyd RD. Mechanical determinants of osteoarthrosiS. Semin Arthritis Rheum 1991;21(Suppl 2):12-21. 17. Altman R, Asch E, Bloch D et al. Development of criteria for the classification and reporting of osteoarthritis: classification of osteoarthritis of the knee. A r t h r i t i s R h e u m 1986;29:1039-1049. 18. Spector TD, H a r t DJ, Byrne J, Harris PA, Dacre JE. Defining the presence of osteoarthritis of the knee in epidemiologic studies. A r t h r i t i s Rheum 1992;35:$82 (abstract). 19. Altman R, Alarcon G, Appelrouth D et al. The American College of R h e u m a t o l o g y criteria for classification and reporting of osteoarthritis of the hip. A r t h r i t i s R h e u m 1991;34:505-5][4. 20. Kallman DA, Wigley FM, Scott WW, Hochberg M, Tobin JD. New radiographic grading scales of osteoarthritis of the hand. A r t h r i t i s R h e u m 1989;32:1584-91. 21. Altman R: Alarcon G, Appelrouth D et al. The American College of Rheumatology criteria for the classification and reporting of osteoarthritis of the hand. A r t h r i t i s R h e u m 1990;33:1601-10. 22. Scott JC, Nevitt MC, Lane WE, Genant HK, Hochberg MC. Association of individual radiographic features of hip osteoarthr~tis with pain. A r t h r i t i s R h e u m 1992;35:$81 (abstract).